Amoebiasis

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Amoebiasis
Other namesAmoebic dysentery, amebiasis, entamoebiasis [1]
Amebiasis LifeCycle.gif
The life-cycle of various intestinal Entamoeba species
Specialty Infectious disease
Symptoms Bloody diarrhea, abdominal pain [2]
Complications Severe colitis, colonic perforation, anemia [2]
Causes Entamoeba histolytica [2]
Diagnostic method Stool examination, antibodies in the blood [2]
Differential diagnosis Bacterial colitis [2]
PreventionImproved sanitation [2]
TreatmentTissue disease: metronidazole, tinidazole, nitazoxanide, dehydroemetine, chloroquine,
Intestinal infection: diloxanide furoate, iodoquinoline [2]
Frequency~480 million [2]

Amoebiasis, or amoebic dysentery, is an infection of the intestines caused by a parasitic amoeba Entamoeba histolytica . [3] [4] Amoebiasis can be present with no, mild, or severe symptoms. [2] Symptoms may include lethargy, loss of weight, colonic ulcerations, abdominal pain, diarrhea, or bloody diarrhea. [5] [2] Complications can include inflammation and ulceration of the colon with tissue death or perforation, which may result in peritonitis. [2] Anemia may develop due to prolonged gastric bleeding. [2]

Contents

Cysts of Entamoeba can survive for up to a month in soil or for up to 45 minutes under fingernails. [2] Invasion of the intestinal lining results in bloody diarrhea. [2] If the parasite reaches the bloodstream it can spread through the body, most frequently ending up in the liver where it can cause amoebic liver abscesses. [2] Liver abscesses can occur without previous diarrhea. [2] Diagnosis is made by stool examination using microscopy, but it can be difficult to distinguish E. hystolitica from other harmless entamoeba species. [3] An increased white blood cell count may be present in severe cases. [2] The most accurate test is finding specific antibodies in the blood, but it may remain positive following treatment. [2] Bacterial colitis can result in similar symptoms. [2]

Prevention of amoebiasis is by improved sanitation, including separating food and water from faeces. [2] There is no vaccine. [2] There are two treatment options depending on the location of the infection. [2] Amoebiasis in tissues is treated with either metronidazole, tinidazole, nitazoxanide, dehydroemetine or chloroquine. Luminal infection is treated with diloxanide furoate or iodoquinoline. [2] Effective treatment against all stages of the disease may require a combination of medications. [2] Infections without symptoms may be treated with just one antibiotic, and infections with symptoms are treated with two antibiotics. [3]

Amoebiasis is present all over the world, [6] though most cases occur in the developing world. [7] About 480 million people are currently infected with about 40 million new cases per year with significant symptoms. [2] [8] This results in the death of between 40,000–100,000 people a year. [4] The first case of amoebiasis was documented in 1875. In 1891, the disease was described in detail, resulting in the terms amoebic dysentery and amoebic liver abscess. [2] Further evidence from the Philippines in 1913 found that upon swallowing cysts of E. histolytica volunteers developed the disease. [2]

Signs and symptoms

Most infected people, about 90%, are asymptomatic, [9] but this disease has the potential to become serious. It is estimated that about 40,000 to 100,000 people worldwide die annually due to amoebiasis. [4]

Infections can sometimes last for years if there is no treatment. Symptoms take from a few days to a few weeks to develop and manifest themselves, but usually it is about two to four weeks. Symptoms can range from mild diarrhea to dysentery with blood, coupled with intense abdominal pains. Extra-intestinal complications might also arise as a result of invasive infection which includes colitis, liver, lung, or brain abscesses. [9] The blood comes from bleeding lesions created by the amoebae invading the lining of the colon. In about 10% of invasive cases the amoebae enter the bloodstream and may travel to other organs in the body. Most commonly this means the liver, [10] as this is where blood from the intestine reaches first, but they can end up almost anywhere in the body.[ citation needed ]

Onset time is highly variable and the average asymptomatic infection persists for over a year. It is theorized that the absence of symptoms or their intensity may vary with such factors as strain of amoeba, immune response of the host, and perhaps associated bacteria and viruses.[ citation needed ]

In asymptomatic infections, the amoeba lives by eating and digesting bacteria and food particles in the gut, a part of the gastrointestinal tract. [9] It does not usually come in contact with the intestine itself due to the protective layer of mucus that lines the gut. Disease occurs when amoeba comes in contact with the cells lining the intestine. It then secretes the same substances it uses to digest bacteria, which include enzymes that destroy cell membranes and proteins. This process can lead to penetration and digestion of human tissues, resulting first in flask-shaped ulcerations in the intestine. Entamoeba histolytica ingests the destroyed cells by phagocytosis and is often seen with red blood cells (a process known as erythrophagocytosis) inside when viewed in stool samples. Especially in Latin America,[ citation needed ] a granulomatous mass (known as an amoeboma) may form in the wall of the ascending colon or rectum due to long-lasting immunological cellular response, and is sometimes confused with cancer. [11]

The ingestion of one viable cyst may cause an infection. [12]

Steroid therapy can occasionally provoke severe amoebic colitis in people with any E. histolytica infection. [13] This bears high mortality: on average more than 50% with severe colitis die. [13]

Cause

Amoebiasis is an infection caused by the amoeba Entamoeba histolytica .

Transmission

Life-cycle of the Entamoeba histolytica Entamoeba histolytica life cycle-en.svg
Life-cycle of the Entamoeba histolytica

Amoebiasis is usually transmitted by the fecal-oral route, [9] but it can also be transmitted indirectly through contact with dirty hands or objects as well as by anal-oral contact. Infection is spread through ingestion of the cyst form of the parasite, a semi-dormant and hardy structure found in feces. Any non-encysted amoebae, or trophozoites , die quickly after leaving the body but may also be present in stool: these are rarely the source of new infections. [9] Since amoebiasis is transmitted through contaminated food and water, it is often endemic in regions of the world with limited modern sanitation systems, including México, Central America, western South America, South Asia, and western and southern Africa. [14]

Amoebic dysentery is one form of traveler's diarrhea, [15] although most traveler's diarrhea is bacterial or viral in origin.

Pathogenesis

Tissue damage caused by E. histolytica is a result of three main events, host cell death, inflammation, and parasite invasion. Abbreviations: EhMIF, E. histolytica macrophage migration inhibitory factor; MMP, matrix metalloproteinases. Tissue damage caused by E. histolytica is a result of three main events, host cell death, inflammation, and parasite invasion.png
Tissue damage caused by E. histolytica is a result of three main events, host cell death, inflammation, and parasite invasion. Abbreviations: EhMIF, E. histolytica macrophage migration inhibitory factor; MMP, matrix metalloproteinases.

Amoebiasis results from tissue destruction induced by the E. histolytica parasite.

E. histolytica causes tissue damage by three main events: direct host cell killing, inflammation, and parasite invasion. [16] The pathogenesis of amoebiasis involves interplay of various molecules secreted by E. histolytica such as LPPG, lectins, cysteine proteases, and amoebapores. Lectins help in the attachment of the parasite to the mucosal layer of the host during invasion. The amoebapores destroy the ingested bacteria present in the colonic environment. Cysteine proteases lyse the host tissues. Other molecules such as PATMK, myosins, G proteins, C2PK, CaBP3, and EhAK1 play an important role in the process of phagocytosis. [17]

Diagnosis

With colonoscopy it is possible to detect small ulcers of between 3–5mm, but diagnosis may be difficult as the mucous membrane between these areas can look either healthy or inflamed. [2] Trophozoites may be identified at the ulcer edge or within the tissue, using immunohistochemical staining with specific anti-E. histolytica antibodies. [7]

Asymptomatic human infections are usually diagnosed by finding cysts shed in the stool. Various flotation or sedimentation procedures have been developed to recover the cysts from fecal matter and stains help to visualize the isolated cysts for microscopic examination. Since cysts are not shed constantly, a minimum of three stools are examined. In symptomatic infections, the motile form (the trophozoite) is often seen in fresh feces. Serological tests exist, and most infected individuals (with symptoms or not) test positive for the presence of antibodies. The levels of antibody are much higher in individuals with liver abscesses. Serology only becomes positive about two weeks after infection. More recent developments include a kit that detects the presence of amoeba proteins in the feces, and another that detects ameba DNA in feces. These tests are not in widespread use due to their expense.[ citation needed ]

Microscopy is still by far the most widespread method of diagnosis around the world. However it is not as sensitive or accurate in diagnosis as the other tests available. It is important to distinguish the E. histolytica cyst from the cysts of nonpathogenic intestinal protozoa such as Entamoeba coli by its appearance. E. histolytica cysts have a maximum of four nuclei, while the commensal Entamoeba coli cyst has up to 8 nuclei. Additionally, in E. histolytica, the endosome is centrally located in the nucleus, while it is usually off-center in Entamoeba coli. Finally, chromatoidal bodies in E. histolytica cysts are rounded, while they are jagged in Entamoeba coli. However, other species, Entamoeba dispar and E. moshkovskii, are also commensals and cannot be distinguished from E. histolytica under the microscope. As E. dispar is much more common than E. histolytica in most parts of the world this means that there is a lot of incorrect diagnosis of E. histolytica infection taking place. The WHO recommends that infections diagnosed by microscopy alone should not be treated if they are asymptomatic and there is no other reason to suspect that the infection is actually E. histolytica. Detection of cysts or trophozoites stools under microscope may require examination of several samples over several days to determine if they are present, because cysts are shed intermittently and may not show up in every sample.[ citation needed ]

Typically, the organism can no longer be found in the feces once the disease goes extra-intestinal.[ citation needed ] Serological tests are useful in detecting infection by E. histolytica if the organism goes extra-intestinal and in excluding the organism from the diagnosis of other disorders. An Ova & Parasite (O&P) test or an E. histolytica fecal antigen assay is the proper assay for intestinal infections. Since antibodies may persist for years after clinical cure, a positive serological result may not necessarily indicate an active infection. A negative serological result, however, can be equally important in excluding suspected tissue invasion by E. histolytica.[ citation needed ]

Stool antigen detection tests have helped to overcome some of the limitations of stool microscopy. Antigen detection tests are easy to use, but they have variable sensitivity and specificity, especially in low-endemic areas. [7]

Polymerase chain reaction (PCR) is considered the gold standard for diagnosis but remains underutilized. [7] [18]

Prevention

Specimen of the human intestine that was damaged by amebic ulcer. Amoebic Ulcer Intestine.jpg
Specimen of the human intestine that was damaged by amebic ulcer.

To help prevent the spread of amoebiasis around the home :[ citation needed ]

To help prevent infection:[ citation needed ]

Good sanitary practice, as well as responsible sewage disposal or treatment, are necessary for the prevention of E. histolytica infection on an endemic level. E.histolytica cysts are usually resistant to chlorination, therefore sedimentation and filtration of water supplies are necessary to reduce the incidence of infection. [9]

E. histolytica cysts may be recovered from contaminated food by methods similar to those used for recovering Giardia lamblia cysts from feces. Filtration is probably the most practical method for recovery from drinking water and liquid foods. E. histolytica cysts must be distinguished from cysts of other parasitic (but nonpathogenic) protozoa and from cysts of free-living protozoa as discussed above. Recovery procedures are not very accurate; cysts are easily lost or damaged beyond recognition, which leads to many falsely negative results in recovery tests. [19]

Treatment

E. histolytica infections occur in both the intestine and (in people with symptoms) in tissue of the intestine and/or liver. [14] Those with symptoms require treatment with two medications, an amoebicidal tissue-active agent and a luminal cysticidal agent. [9] Individuals that are asymptomatic only need a luminal cysticidal agent. [7]

Prognosis

Significance of Amebiasis Significance of Amebiasis.png
Significance of Amebiasis

In the majority of cases, amoebas remain in the gastrointestinal tract of the hosts. Severe ulceration of the gastrointestinal mucosal surfaces occurs in less than 16% of cases. In fewer cases, the parasite invades the soft tissues, most commonly the liver. [10] Only rarely are masses formed (amoebomas) that lead to intestinal obstruction.(Mistaken for Ca caecum and appendicular mass) Other local complications include bloody diarrhea, pericolic and pericaecal abscess.[ citation needed ]

Complications of hepatic amoebiasis includes subdiaphragmatic abscess, perforation of diaphragm to pericardium and pleural cavity, perforation to abdominal cavital (amoebic peritonitis) and perforation of skin (amoebiasis cutis).[ citation needed ]

Pulmonary amoebiasis can occur from liver lesions by spread through the blood or by perforation of pleural cavity and lung. It can cause lung abscess, pulmono pleural fistula, empyema lung and broncho pleural fistula. It can also reach the brain through blood vessels and cause amoebic brain abscess and amoebic meningoencephalitis. Cutaneous amoebiasis can also occur in skin around sites of colostomy wound, perianal region, region overlying visceral lesion and at the site of drainage of liver abscess.[ citation needed ]

Urogenital tract amoebiasis derived from intestinal lesion can cause amoebic vulvovaginitis (May's disease), rectovesicle fistula and rectovaginal fistula.[ citation needed ]

Entamoeba histolytica infection is associated with malnutrition and stunting of growth in children. [20]

Epidemiology

Amoebiasis caused about 55,000 deaths worldwide in 2010, down from 68,000 in 1990. [21] [22] In older textbooks it is often stated that 10% of the world's population is infected with Entamoeba histolytica .[ citation needed ] Nevertheless, this means that there are up to 50 million true E. histolytica infections and approximately seventy thousand die each year, mostly from liver abscesses or other complications. Although usually considered a tropical parasite, the first case reported (in 1875) was actually in St Petersburg in Russia, near the Arctic Circle. [23] Infection is more common in warmer areas, but this is because of both poorer hygiene and the parasitic cysts surviving longer in warm moist conditions. [14]

History

Amoebiasis was first described by Fedor A. Lösch in 1875, in northern Russia. [2] [9] The most dramatic incident in the US was the Chicago World's Fair outbreak in 1933, caused by contaminated drinking water. There were more than a thousand cases, with 98 deaths. [24] [25] It has been known since 1897 that at least one non-disease-causing species of Entamoeba existed (Entamoeba coli), but it was first formally recognized by the WHO in 1997 that E. histolytica was two species, despite this having first been proposed in 1925. [2] In addition to the now-recognized E. dispar, evidence shows there are at least two other species of Entamoeba that look the same in humans: E. moshkovskii and Entamoeba bangladeshi. [2] The reason these species haven't been differentiated until recently is because of the reliance on appearance. [2]

Joel Connolly of the Chicago Bureau of Sanitary Engineering brought the outbreak to an end when he found that defective plumbing permitted sewage to contaminate drinking water. In 1998 there was an outbreak of amoebiasis in the Republic of Georgia. [26] Between 26 May and 3 September 1998, 177 cases were reported, including 71 cases of intestinal amoebiasis and 106 probable cases of liver abscess.[ citation needed ]

The Nicobarese people have attested to the medicinal properties found in Glochidion calocarpum , a plant common to India, saying that its bark and seed are most effective in curing abdominal disorders associated with amoebiasis. [27]

Society and culture

An outbreak of amoebic dysentery occurs in Diana Gabaldon's novel A Breath of Snow and Ashes . [28]

Related Research Articles

<i>Entamoeba</i> Genus of internal parasites

Entamoeba is a genus of Amoebozoa found as internal parasites or commensals of animals. In 1875, Fedor Lösch described the first proven case of amoebic dysentery in St. Petersburg, Russia. He referred to the amoeba he observed microscopically as Amoeba coli; however, it is not clear whether he was using this as a descriptive term or intended it as a formal taxonomic name. The genus Entamoeba was defined by Casagrandi and Barbagallo for the species Entamoeba coli, which is known to be a commensal organism. Lösch's organism was renamed Entamoeba histolytica by Fritz Schaudinn in 1903; he later died, in 1906, from a self-inflicted infection when studying this amoeba. For a time during the first half of the 20th century the entire genus Entamoeba was transferred to Endamoeba, a genus of amoebas infecting invertebrates about which little is known. This move was reversed by the International Commission on Zoological Nomenclature in the late 1950s, and Entamoeba has stayed 'stable' ever since.

<span class="mw-page-title-main">Dysentery</span> Inflammation of the intestine causing diarrhea with blood

Dysentery, historically known as the bloody flux, is a type of gastroenteritis that results in bloody diarrhea. Other symptoms may include fever, abdominal pain, and a feeling of incomplete defecation. Complications may include dehydration.

<i>Entamoeba histolytica</i> Anaerobic parasitic protist

Entamoeba histolytica is an anaerobic parasitic amoebozoan, part of the genus Entamoeba. Predominantly infecting humans and other primates causing amoebiasis, E. histolytica is estimated to infect about 35-50 million people worldwide. E. histolytica infection is estimated to kill more than 55,000 people each year. Previously, it was thought that 10% of the world population was infected, but these figures predate the recognition that at least 90% of these infections were due to a second species, E. dispar. Mammals such as dogs and cats can become infected transiently, but are not thought to contribute significantly to transmission.

<i>Entamoeba coli</i> Species of parasitic amoeba

Entamoeba coli is a non-pathogenic species of Entamoeba that frequently exists as a commensal parasite in the human gastrointestinal tract. E. coli is important in medicine because it can be confused during microscopic examination of stained stool specimens with the pathogenic Entamoeba histolytica. This amoeba does not move much by the use of its pseudopod, and creates a "sur place (non-progressive) movement" inside the large intestine. Usually, the amoeba is immobile, and keeps its round shape. This amoeba, in its trophozoite stage, is only visible in fresh, unfixed stool specimens. Sometimes the Entamoeba coli have parasites as well. One is the fungus Sphaerita spp. This fungus lives in the cytoplasm of the E. coli. While this differentiation is typically done by visual examination of the parasitic cysts via light microscopy, new methods using molecular biology techniques have been developed. The scientific name of the amoeba, E. coli, is often mistaken for the bacterium, Escherichia coli. Unlike the bacterium, the amoeba is mostly harmless, and does not cause as many intestinal problems as some strains of the E. coli bacterium. To make the naming of these organisms less confusing, "alternate contractions" are used to name the species for the purpose making the naming easier; for example, using Esch. coli and Ent. coli for the bacterium and amoeba, instead of using E. coli for both.

<span class="mw-page-title-main">Amoebozoa</span> Phylum of protozoans

Amoebozoa is a major taxonomic group containing about 2,400 described species of amoeboid protists, often possessing blunt, fingerlike, lobose pseudopods and tubular mitochondrial cristae. In traditional classification schemes, Amoebozoa is usually ranked as a phylum within either the kingdom Protista or the kingdom Protozoa. In the classification favored by the International Society of Protistologists, it is retained as an unranked "supergroup" within Eukaryota. Molecular genetic analysis supports Amoebozoa as a monophyletic clade. Modern studies of eukaryotic phylogenetic trees identify it as the sister group to Opisthokonta, another major clade which contains both fungi and animals as well as several other clades comprising some 300 species of unicellular eukaryotes. Amoebozoa and Opisthokonta are sometimes grouped together in a high-level taxon, variously named Unikonta, Amorphea or Opimoda.

A trophozoite is the activated, feeding stage in the life cycle of certain protozoa such as malaria-causing Plasmodium falciparum and those of the Giardia group. The complementary form of the trophozoite state is the thick-walled cyst form. They are often different from the cyst stage, which is a protective, dormant form of the protozoa. Trophozoites are often found in the host's body fluids and tissues and in many cases, they are the form of the protozoan that causes disease in the host. In the protozoan, Entamoeba histolytica it invades the intestinal mucosa of its host, causing dysentery, which aid in the trophozoites traveling to the liver and leading to the production of hepatic abscesses.

Dientamoebiasis is a medical condition caused by infection with Dientamoeba fragilis, a single-cell parasite that infects the lower gastrointestinal tract of humans. It is an important cause of traveler's diarrhea, chronic abdominal pain, chronic fatigue, and failure to thrive in children.

<span class="mw-page-title-main">Diloxanide</span> Medication for amoebic gut infections

Diloxanide is a medication used to treat amoeba infections. In places where infections are not common, it is a second line treatment after paromomycin when a person has no symptoms. For people who are symptomatic, it is used after treatment with metronidazole or tinidazole. It is taken by mouth.

<span class="mw-page-title-main">Protozoan infection</span> Parasitic disease caused by a protozoan

Protozoan infections are parasitic diseases caused by organisms formerly classified in the kingdom Protozoa. These organisms are now classified in the supergroups Excavata, Amoebozoa, Harosa, and Archaeplastida. They are usually contracted by either an insect vector or by contact with an infected substance or surface.

An amebicide is an agent that is destructive to amoeba, especially parasitic amoeba that cause amoebiasis.

<span class="mw-page-title-main">Amoebic liver abscess</span> Medical condition

A amoebic liver abscess is a type of liver abscess caused by amebiasis. It is the involvement of liver tissue by trophozoites of the organism Entamoeba histolytica and of its abscess due to necrosis.

<span class="mw-page-title-main">Amoebic brain abscess</span> Medical condition

Amoebic brain abscess is an affliction caused by the anaerobic parasitic protist Entamoeba histolytica. It is extremely rare; the first case being reported in 1849. Brain abscesses resulting from Entamoeba histolytica are difficult to diagnose and very few case reports suggest complete recovery even after the administration of appropriate treatment regimen.

Cutaneous amoebiasis, refers to a form of amoebiasis that presents primarily in the skin. It can be caused by Acanthamoeba or Entamoeba histolytica. When associated with Acanthamoeba, it is also known as "cutaneous acanthamoebiasis". Balamuthia mandrillaris can also cause cutaneous amoebiasis, but can prove fatal if the amoeba enters the bloodstream It is characterized by ulcers. Diagnosis of amebiasis cutis calls for high degree of clinical suspicion. This needs to be backed with demonstration of trophozoites from lesions. Unless an early diagnosis can be made such patients can develop significant morbidity.

<span class="mw-page-title-main">Dehydroemetine</span> Chemical compound

Dehydroemetine is a synthetically produced antiprotozoal agent similar to emetine in its anti-amoebic properties and structure, but it produces fewer side effects. In the United States, it is manufactured by Roche.

Entamoeba polecki is an intestinal parasite of the genus Entamoeba. E. polecki is found primarily in pigs and monkeys and is largely considered non-pathogenic in humans, although there have been some reports regarding symptomatic infections of humans. Prevalence is concentrated in New Guinea, with distribution also recorded in areas of southeast Asia, France, and the United States.

<i>Dientamoeba fragilis</i> Parasite of humans, pigs and gorillas

Dientamoeba fragilis is a species of single-celled excavates found in the gastrointestinal tract of some humans, pigs and gorillas. It causes gastrointestinal upset in some people, but not in others. It is an important cause of travellers diarrhoea, chronic diarrhoea, fatigue and, in children, failure to thrive. Despite this, its role as a "commensal, pathobiont, or pathogen" is still debated. D. fragilis is one of the smaller parasites that are able to live in the human intestine. Dientamoeba fragilis cells are able to survive and move in fresh feces but are sensitive to aerobic environments. They dissociate when in contact or placed in saline, tap water or distilled water.

<i>Cystoisospora belli</i> Species of single-celled organism

Cystoisospora belli, previously known as Isospora belli, is a parasite that causes an intestinal disease known as cystoisosporiasis. This protozoan parasite is opportunistic in immune suppressed human hosts. It primarily exists in the epithelial cells of the small intestine, and develops in the cell cytoplasm. The distribution of this coccidian parasite is cosmopolitan, but is mainly found in tropical and subtropical areas of the world such as the Caribbean, Central and S. America, India, Africa, and S.E. Asia. In the U.S., it is usually associated with HIV infection and institutional living.

Entamoeba moshkovskii is part of the genus Entamoeba. It is found in areas with polluted water sources, and is prevalent in places such as Malaysia, India, and Bangladesh, but more recently has made its way to Turkey, Australia, and North America. This amoeba is said to rarely infect humans, but recently this has changed. It is in question as to whether it is pathogenic or not. Despite some sources stating this is a free living amoeba, various studies worldwide have shown it contains the ability to infect humans, with some cases of pathogenic potential being reported. Some of the symptoms that often occur are diarrhea, weight loss, bloody stool, and abdominal pain. The first known human infection also known as the "Laredo strain" of Entamoebic mushkovskii was in Laredo, Texas in 1991, although it was first described by a man named Tshalaia in 1941 in Moscow, Russia. It is known to affect people of all ages and genders.

Entamoeba invadens is an amoebozoa parasite of reptiles, within the genus Entamoeba. It is closely related to the human parasite Entamoeba histolytica, causing similar invasive disease in reptiles, in addition to a similar morphology and lifecycle.

<i>Naegleria fowleri</i> Species of free-living excavate form of protist

Naegleria fowleri, colloquially known as the brain-eating amoeba, is a species of the genus Naegleria. It belongs to the phylum Percolozoa and is technically classified as an amoeboflagellate excavate, rather than a true amoeba. This free-living microorganism primarily feeds on bacteria but can become pathogenic in humans, causing an extremely rare, sudden, severe, and usually fatal brain infection known as naegleriasis or primary amoebic meningoencephalitis (PAM).

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  27. ↑ See p. 412 in: Hammer K (1990). "Barilla (Salsola soda, Chenopodiaceae)". Economic Botany. 44 (3): 410–412. doi:10.1007/bf03183925. JSTOR   4255259. S2CID   32113455.
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